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Nagoshi graduated with a degree in movie production and joined Sega shortly thereafter, working for the second arcade department (AM2) at Sega under Yu Suzuki as a CG designer.[4] His first title was Virtua Racing as a chief designer. Afterwards he created his own racing game, Daytona USA, where he was producer, director and chief designer. He created more arcade racing games with Scud Race in 1996 and Daytona USA 2 in 1998.[5] By 1998, Nagoshi had his own arcade department, where he worked on SpikeOut.

In 2000, Sega separated its in-house R&D departments from the main company and established them in nine semi-autonomous subsidiaries, with each getting an elected president as a studio head. Toshihiro Nagoshi became head of Amusement Vision, where he further contributed to Sega's arcade line-up with Planet Harriers, SpikeOut sequels and spin-offs. For Dreamcast he remade his very first game, Daytona USA as Daytona USA 2001. As Sega became a third-party, he moved out of arcade development. Amusement Vision became most known for its work on the Nintendo GameCube, with the first two Super Monkey Ball titles in 2001 and 2002, and F-Zero GX in 2003, Nagoshi made in conjunction with Shigeru Miyamoto. During the time of development of F-Zero GX, Nagoshi wrote a regular column in Edge, which was titled "AV Out" in reference to both Amusement Vision's initials, which was the name of his development division, and the consumer electronics term "A/V".

In 2003, major changes took place at Sega, consolidating much of their studios. Nagoshi was appointed to the group of the company's officers.[6] In 2005, he was in charge of the New Entertainment Division at Sega, which housed both his prior team, with the addition of staff that worked on Jet Set Radio, Panzer Dragoon Orta and GunValkyrie, that already produced the Ollie King arcade release at Amusement Vision.

Nagoshi launched his Yakuza franchise. The first title cost $21 million to produce and the first PlayStation 3 entry, Ryū ga Gotoku Kenzan! was more expensive, with Nagoshi stating that it his biggest production since he started working on consumer games.[7] By 2009, New Entertainment diminished, and Nagoshi became the R&D Creative Officer of Sega of Japan's Consumer Division.[8]

In February 2012 it was announced that Nagoshi would be promoted to the role of chief creative officer at Sega of Japan, as well as being appointed to the company's board of directors. He took up these positions on April 1, 2012.[9] In October 2013, once Sega Sammy purchased the bankrupt Index Corporation under the shell corporation, Sega Dream Corporation, Nagoshi was appointed as a member of the board of directors for the reformed Atlus.[10]